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  • 1
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    In situ identification and N2 and C fixation rates of uncultivated cyanobacteria populations (2013)
    Elsevier
    In:  Systematic and Applied Microbiology, 36 (4). pp. 259-271.
    Details
    Publication Date: 2019-06-27
    Description: Nitrogen (N-2) fixation is a globally important process often mediated by diazotrophic cyanobacteria in the open ocean. In 2010, seawater was collected near Cape Verde to identify and measure N-2 and carbon (C) fixation by unicellular diazotrophic cyanobacteria. The nifH gene abundance (10(4)-10(6) nifH L-1) and nifH gene transcript abundance (10(2)-10(4) cDNA nifH L-1) for two unicellular groups, UCYN-A and UCYN-B, were detected. UCYN-A was also identified and quantified (10(4)-10(3) cells L-1) by new probes (UCYN-A732 and UCYN-A159) using Catalyzed Reporter Deposition-Fluorescence In Situ Hybridization (CARD-FISH) assays. The UCYN-A were observed as free cells or attached to a larger unidentified eukaryotic cell. A Halogen In Situ Hybridization-Secondary Ion Mass Spectrometry (HISH-SIMS) assay using the UCYN-A732 probe was applied on samples previously incubated with C-13-bicarbonate and N-15(2). Free UCYN-A cells were enriched in both C-13 and N-15 and estimated C and N-2 fixation rates for UCYN-A were lower compared to co-occurring unicellular cyanobacteria cells similar in size (3.1-5.6 mu m) and pigmentation to diazotroph Crocosphaera watsonii. Here, we identify and quantify two common co-occurring unicellular groups and measure their cellular activities by nanoSIMS
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1016/j.syapm.2013.02.002
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  • 2
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    Resolution of Conflicting Signals at the Single-Cell Level in the Regulation of Cyanobacterial Photosynthesis and Nitrogen Fixation (2013)
    Public Library of Science
    In:  PLoS ONE, 8 (6). e66060.
    Details
    Publication Date: 2017-06-22
    Description: Unicellular, diazotrophic cyanobacteria temporally separate dinitrogen (N-2) fixation and photosynthesis to prevent inactivation of the nitrogenase by oxygen. This temporal segregation is regulated by a circadian clock with oscillating activities of N-2 fixation in the dark and photosynthesis in the light. On the population level, this separation is not always complete, since the two processes can overlap during transitions from dark to light. How do single cells avoid inactivation of nitrogenase during these periods? One possibility is that phenotypic heterogeneity in populations leads to segregation of the two processes. Here, we measured N-2 fixation and photosynthesis of individual cells using nanometer-scale secondary ion mass spectrometry (nanoSIMS) to assess both processes in a culture of the unicellular, diazotrophic cyanobacterium Crocosphaera watsonii during a dark-light and a continuous light phase. We compared single-cell rates with bulk rates and gene expression profiles. During the regular dark and light phases, C. watsonii exhibited the temporal segregation of N-2 fixation and photosynthesis commonly observed. However, N-2 fixation and photosynthesis were concurrently measurable at the population level during the subjective dark phase in which cells were kept in the light rather than returned to the expected dark phase. At the single-cell level, though, cells discriminated against either one of the two processes. Cells that showed high levels of photosynthesis had low nitrogen fixing activities, and vice versa. These results suggest that, under ambiguous environmental signals, single cells discriminate against either photosynthesis or nitrogen fixation, and thereby might reduce costs associated with running incompatible processes in the same cell.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1371/journal.pone.0066060
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  • 3
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    Doubling of marine dinitrogen-fixation rates based on direct measurements (2012)
    Nature Publishing Group
    In:  Nature, 488 . pp. 361-364.
    Details
    Publication Date: 2017-03-09
    Description: Biological dinitrogen fixation provides the largest input of nitrogen to the oceans, therefore exerting important control on the ocean’s nitrogen inventory and primary productivity. Nitrogen-isotope data fromocean sediments suggest that the marine-nitrogen inventory has been balanced for the past 3,000 years (ref. 4). Producing a balanced marine-nitrogenbudget based on direct measurements has proved difficult, however, with nitrogen loss exceeding the gain from dinitrogen fixation by approximately 200 TgNyr-1 (refs 5, 6). Here we present data from the Atlantic Ocean and show that the most widely used method of measuring oceanic N2-fixation rates underestimates the contribution of N2-fixing microorganisms (diazotrophs) relative to a newly developed method. Using molecular techniques to quantify the abundance of specific clades of diazotrophs in parallel with rates of 15N2 incorporation into particulate organic matter, we suggest that the difference between N2-fixation rates measured with the established method and those measured with the new method8 can be related to the composition of the diazotrophic community. Our data show that in areas dominated by Trichodesmium, the established method underestimatesN2-fixation rates by an averageof 62%. We also find that the newly developed method yields N2-fixation rates more than six times higher than those from the established method when unicellular, symbiotic cyanobacteria and c-proteobacteria dominate the diazotrophic community. On the basis of average areal rates measured over the Atlantic Ocean, we calculated basin-wide N2-fixation rates of 14+/-1TgNyr-1 and 24+/-1TgNyr-1 for the established and new methods, respectively. If our findings can be extrapolated to other ocean basins, this suggests that the global marine N2-fixation rate derived from direct measurements may increase from 103+/-8TgNyr-1 to 177+/-8TgNyr-1, and that the contribution of N2 fixers other than Trichodesmium is much more significant than was previously thought.
    Type: Article , PeerReviewed
    Format: text
    Format: text
    DOI: 10.1038/nature11338
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  • 4
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    Methodological Underestimation of Oceanic Nitrogen Fixation Rates (2010)
    Public Library of Science
    In:  PLoS ONE, 5 (9). e12583.
    Details
    Publication Date: 2019-09-23
    Description: The two commonly applied methods to assess dinitrogen (N2) fixation rates are the 15N2-tracer addition and the acetylene reduction assay (ARA). Discrepancies between the two methods as well as inconsistencies between N2 fixation rates and biomass/growth rates in culture experiments have been attributed to variable excretion of recently fixed N2. Here we demonstrate that the 15N2-tracer addition method underestimates N2 fixation rates significantly when the 15N2 tracer is introduced as a gas bubble. The injected 15N2 gas bubble does not attain equilibrium with the surrounding water leading to a 15N2 concentration lower than assumed by the method used to calculate 15N2-fixation rates. The resulting magnitude of underestimation varies with the incubation time, to a lesser extent on the amount of injected gas and is sensitive to the timing of the bubble injection relative to diel N2 fixation patterns. Here, we propose and test a modified 15N2 tracer method based on the addition of 15N2-enriched seawater that provides an instantaneous, constant enrichment and allows more accurate calculation of N2 fixation rates for both field and laboratory studies. We hypothesise that application of N2 fixation measurements using this modified method will significantly reduce the apparent imbalances in the oceanic fixed-nitrogen budget.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1371/journal.pone.0012583
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  • 5
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    The small unicellular diazotrophic symbiont, UCYN-A, is a key player in the marine nitrogen cycle (2016)
    Nature Research
    In:  Nature Microbiology, 1 . Art. No. 16163.
    Details
    Publication Date: 2019-09-23
    Description: Microbial dinitrogen (N2) fixation, the nitrogenase enzyme-catalysed reduction of N2 gas into biologically available ammonia, is the main source of new nitrogen (N) in the ocean. For more than 50 years, oceanic N2 fixation has mainly been attributed to the activity of the colonial cyanobacterium Trichodesmium1,2. Other smaller N2-fixing microorganisms (diazotrophs)—in particular the unicellular cyanobacteria group A (UCYN-A)—are, however, abundant enough to potentially contribute significantly to N2 fixation in the surface waters of the oceans3,​4,​5,​6. Despite their abundance, the contribution of UCYN-A to oceanic N2 fixation has so far not been directly quantified. Here, we show that in one of the main areas of oceanic N2 fixation, the tropical North Atlantic7, the symbiotic cyanobacterium UCYN-A contributed to N2 fixation similarly to Trichodesmium. Two types of UCYN-A, UCYN-A1 and -A2, were observed to live in symbioses with specific eukaryotic algae. Single-cell analyses showed that both algae–UCYN-A symbioses actively fixed N2, contributing ∼20% to N2 fixation in the tropical North Atlantic, revealing their significance in this region. These symbioses had growth rates five to ten times higher than Trichodesmium, implying a rapid transfer of UCYN-A-fixed N into the food web that might significantly raise their actual contribution to N2 fixation. Our analysis of global 16S rRNA gene databases showed that UCYN-A occurs in surface waters from the Arctic to the Antarctic Circle and thus probably contributes to N2 fixation in a much larger oceanic area than previously thought. Based on their high rates of N2 fixation and cosmopolitan distribution, we hypothesize that UCYN-A plays a major, but currently overlooked role in the oceanic N cycle.
    Type: Article , PeerReviewed
    Format: text
    Format: text
    Format: other
    Format: other
    DOI: 10.1038/nmicrobiol.2016.163
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  • 6
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    The "DARK MATTER" of nitrogen fixation (2011)
    In:  [Talk] In: SAME12 - 12. Symposium on Aquatic Microbial Ecology, 28.08.-02.09.2011, Rostock/Warnemünde, Germany .
    Details
    Publication Date: 2019-09-23
    Description: Biological nitrogen fixation is the largest input of fixed nitrogen into the oceans and thus a key parameter in controlling primary productivity. Despite the importance of nitrogen fixation there is major controversy about its magnitude on a global scale, due to a gap in the marine nitrogen cycle on the input side. While this gap suggests that the nitrogen cycle is currently not in balance and the oceans are losing more nitrogen than they gain, stable isotope measurements from sediment cores suggest that the nitrogen cycle has been in balance over the last 3000 years. To resolve this paradox it has been suggested that marine nitrogen fixation is currently underestimated. We used a revised method to measure nitrogen fixation and compared it with the prior, widely applied method. Our study reveals that over the whole Atlantic Ocean the prior method underestimated nitrogen fixation rates. In certain areas the mean fixationrate increased over six fold when measured with the revised protocol. The magnitude of the difference is not stable but rather highly variable on a coarse geographic scale. We suspected that species composition has a great influence on the magnitude of underestimation of nitrogen fixation rates by the prior method, a theory we could confirm with a laboratory experiment. Taken together, our results imply that there is an urgent need to agree on a common protocol for nitrogen fixation rate measurements to assess the true potential of this nitrogen input process and be able to model the future development, given man-made climate changes
    Type: Conference or Workshop Item , NonPeerReviewed
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  • 7
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    Single-cell analysis of dinitrogen fixation and photosynthesis using nanoSIMS (2010)
    In:  [Poster] In: Gordon Research Conference "Marine Microbes", 04.-09.07.2010, Tilton, New Hampshire, USA .
    Details
    Publication Date: 2012-02-23
    Type: Conference or Workshop Item , NonPeerReviewed
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  • 8
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    N-Limitation of the Phytoplankton Community in the Mediterranean Sea (2011)
    In:  [Poster] In: ASLO Aquatic Sciences Meeting, 13.-18.02.2011, San Juan, Puerto Rico, USA .
    Details
    Publication Date: 2012-03-15
    Type: Conference or Workshop Item , NonPeerReviewed
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  • 9
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    Environmental controls on nitrogen fixation (2009)
    In:  [Talk] In: Treffen des Wissenschaftlichen Beirats, 28.04, Kiel .
    Details
    Publication Date: 2012-02-23
    Type: Conference or Workshop Item , NonPeerReviewed
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  • 10
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    Diel rhythm of nitrogen and carbon metabolism in the unicellular, diazotrophic cyanobacterium Crocosphaera watsonii WH8501 (2010)
    Wiley
    In:  Environmental Microbiology, 12 (2). pp. 412-421.
    Details
    Publication Date: 2018-09-12
    Description: We examined the diel variation in nitrogen and carbon metabolism in Crocosphaera watsonii WH8501 at the physiological and gene expression level in order to determine the temporal constraints for N2 fixation and photosynthesis. N2 fixation and photosynthesis were restricted to the dark and light periods, respectively, during a 24 h light–dark cycle. All genes studied here except one (psbA2) showed diel variations in their expression levels. The highest variation was seen in nifH and nifX relative transcript abundance with a factor of 3–5 × 103 between light and dark periods. Photosynthesis genes showed less variation with a maximum factor of about 500 and always had high relative transcript abundances relative to other genes. At the protein level, the photosystems appeared more stable than the nitrogenase complex over a 24 h light–dark cycle, suggesting that C. watsonii retains the ability to photosynthesize during the dark period of the diel cycle. In contrast, nitrogenase is synthesized daily and exhibits peak abundance during the dark period. Our results have implications for field studies with respect to the interpretation of environmental gene expression data.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1111/j.1462-2920.2009.02078.x
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